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. 1996 Mar 1;491(Pt 2):281–290. doi: 10.1113/jphysiol.1996.sp021215

ATP-activated cation conductance in a Xenopus renal epithelial cell line.

M Mori 1, T Nishizaki 1, K Kawahara 1, Y Okada 1
PMCID: PMC1158725  PMID: 8866854

Abstract

1. Using a whole-cell voltage-clamp technique and fura-2 fluorescence measurements, the actions of extracellular adenosine 5'-triphosphate (ATP) in single cells of an epithelial cell line (A6), were investigated. 2. ATP (0.1-1000 microM) induced currents in cells held under voltage clamp. The sequence of purinergic agonist potency in activating the currents (2-methylthio ATP > adenosine 5'-diphosphate (ADP) > ATP > alpha, beta-methylene ATP) was consistent with that of P2y receptors. 3. Reversal potentials (Erev) of the currents under various ionic conditions suggest that potassium channels and non-selective cation channels were responsible for the ATP-activated conductance, which was permeable to calcium. 4. ATP activated the currents in a calcium-free extracellular solution. In the presence of extracellular calcium, the currents were completely inhibited with 10 mM EGTA in the pipette. 5. ATP (10 microM) increased the intracellular calcium concentration ([Ca2+]i) whether cells were bathed in a solution containing calcium or not. 6. These results indicate that ATP evoked a calcium-dependent cation conductance, permeable to calcium, through P2y receptors by releasing calcium from intracellular stores in A6 cells.

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Selected References

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  1. Adams D. J., Dwyer T. M., Hille B. The permeability of endplate channels to monovalent and divalent metal cations. J Gen Physiol. 1980 May;75(5):493–510. doi: 10.1085/jgp.75.5.493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bacskai B. J., Friedman P. A. Activation of latent Ca2+ channels in renal epithelial cells by parathyroid hormone. Nature. 1990 Sep 27;347(6291):388–391. doi: 10.1038/347388a0. [DOI] [PubMed] [Google Scholar]
  3. Barnard E. A., Burnstock G., Webb T. E. G protein-coupled receptors for ATP and other nucleotides: a new receptor family. Trends Pharmacol Sci. 1994 Mar;15(3):67–70. doi: 10.1016/0165-6147(94)90280-1. [DOI] [PubMed] [Google Scholar]
  4. Bean B. P., Williams C. A., Ceelen P. W. ATP-activated channels in rat and bullfrog sensory neurons: current-voltage relation and single-channel behavior. J Neurosci. 1990 Jan;10(1):11–19. doi: 10.1523/JNEUROSCI.10-01-00011.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Benham C. D., Bolton T. B., Byrne N. G., Large W. A. Action of externally applied adenosine triphosphate on single smooth muscle cells dispersed from rabbit ear artery. J Physiol. 1987 Jun;387:473–488. doi: 10.1113/jphysiol.1987.sp016585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Benham C. D., Tsien R. W. A novel receptor-operated Ca2+-permeable channel activated by ATP in smooth muscle. Nature. 1987 Jul 16;328(6127):275–278. doi: 10.1038/328275a0. [DOI] [PubMed] [Google Scholar]
  7. Burnstock G. Purinergic nerves. Pharmacol Rev. 1972 Sep;24(3):509–581. [PubMed] [Google Scholar]
  8. Burnstock G. Review lecture. Neurotransmitters and trophic factors in the autonomic nervous system. J Physiol. 1981;313:1–35. doi: 10.1113/jphysiol.1981.sp013648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cantiello H. F., Patenaude C. R., Ausiello D. A. G protein subunit, alpha i-3, activates a pertussis toxin-sensitive Na+ channel from the epithelial cell line, A6. J Biol Chem. 1989 Dec 15;264(35):20867–20870. [PubMed] [Google Scholar]
  10. Charest R., Blackmore P. F., Exton J. H. Characterization of responses of isolated rat hepatocytes to ATP and ADP. J Biol Chem. 1985 Dec 15;260(29):15789–15794. [PubMed] [Google Scholar]
  11. Christie A., Sharma V. K., Sheu S. S. Mechanism of extracellular ATP-induced increase of cytosolic Ca2+ concentration in isolated rat ventricular myocytes. J Physiol. 1992 Jan;445:369–388. doi: 10.1113/jphysiol.1992.sp018929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Churchill P. C., Ellis V. R. Purinergic P2y receptors stimulate renin secretion by rat renal cortical slices. J Pharmacol Exp Ther. 1993 Jul;266(1):160–163. [PubMed] [Google Scholar]
  13. Fieber L. A., Adams D. J. Adenosine triphosphate-evoked currents in cultured neurones dissociated from rat parasympathetic cardiac ganglia. J Physiol. 1991 Mar;434:239–256. doi: 10.1113/jphysiol.1991.sp018467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Greenberg S., Di Virgilio F., Steinberg T. H., Silverstein S. C. Extracellular nucleotides mediate Ca2+ fluxes in J774 macrophages by two distinct mechanisms. J Biol Chem. 1988 Jul 25;263(21):10337–10343. [PubMed] [Google Scholar]
  15. Hagiwara S., Ohmori H. Studies of calcium channels in rat clonal pituitary cells with patch electrode voltage clamp. J Physiol. 1982 Oct;331:231–252. doi: 10.1113/jphysiol.1982.sp014371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  17. Hara N., Ichinose M., Sawada M., Imai K., Maeno T. Activation of single Ca2(+)-dependent K+ channel by external ATP in mouse macrophages. FEBS Lett. 1990 Jul 16;267(2):281–284. doi: 10.1016/0014-5793(90)80945-f. [DOI] [PubMed] [Google Scholar]
  18. Hirano Y., Okajima F., Tomura H., Majid M. A., Takeuchi T., Kondo Y. Change of intracellular calcium of neural cells induced by extracellular ATP. FEBS Lett. 1991 Jun 24;284(2):235–237. doi: 10.1016/0014-5793(91)80693-w. [DOI] [PubMed] [Google Scholar]
  19. Inoue R., Brading A. F. The properties of the ATP-induced depolarization and current in single cells isolated from the guinea-pig urinary bladder. Br J Pharmacol. 1990 Jul;100(3):619–625. doi: 10.1111/j.1476-5381.1990.tb15856.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Jope R. S., Song L., Powers R. [3H]PtdIns hydrolysis in postmortem human brain membranes is mediated by the G-proteins Gq/11 and phospholipase C-beta. Biochem J. 1994 Dec 1;304(Pt 2):655–659. doi: 10.1042/bj3040655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lewis C. A. Ion-concentration dependence of the reversal potential and the single channel conductance of ion channels at the frog neuromuscular junction. J Physiol. 1979 Jan;286:417–445. doi: 10.1113/jphysiol.1979.sp012629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Middleton J. P., Mangel A. W., Basavappa S., Fitz J. G. Nucleotide receptors regulate membrane ion transport in renal epithelial cells. Am J Physiol. 1993 May;264(5 Pt 2):F867–F873. doi: 10.1152/ajprenal.1993.264.5.F867. [DOI] [PubMed] [Google Scholar]
  23. Mitchell K. D., Navar L. G. Modulation of tubuloglomerular feedback responsiveness by extracellular ATP. Am J Physiol. 1993 Mar;264(3 Pt 2):F458–F466. doi: 10.1152/ajprenal.1993.264.3.F458. [DOI] [PubMed] [Google Scholar]
  24. Nanoff C., Freissmuth M., Tuisl E., Schütz W. P2-, but not P1-purinoceptors mediate formation of 1, 4, 5-inositol trisphosphate and its metabolites via a pertussis toxin-insensitive pathway in the rat renal cortex. Br J Pharmacol. 1990 May;100(1):63–68. doi: 10.1111/j.1476-5381.1990.tb12052.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. O'Connor S. E., Dainty I. A., Leff P. Further subclassification of ATP receptors based on agonist studies. Trends Pharmacol Sci. 1991 Apr;12(4):137–141. doi: 10.1016/0165-6147(91)90530-6. [DOI] [PubMed] [Google Scholar]
  26. Sasakawa N., Nakaki T., Yamamoto S., Kato R. Stimulation by ATP of inositol trisphosphate accumulation and calcium mobilization in cultured adrenal chromaffin cells. J Neurochem. 1989 Feb;52(2):441–447. doi: 10.1111/j.1471-4159.1989.tb09140.x. [DOI] [PubMed] [Google Scholar]
  27. Schneider P., Hopp H. H., Isenberg G. Ca2+ influx through ATP-gated channels increments [Ca2+]i and inactivates ICa in myocytes from guinea-pig urinary bladder. J Physiol. 1991;440:479–496. doi: 10.1113/jphysiol.1991.sp018720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sela D., Ram E., Atlas D. ATP receptor. A putative receptor-operated channel in PC-12 cells. J Biol Chem. 1991 Sep 25;266(27):17990–17994. [PubMed] [Google Scholar]

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